Full lifetime perspectives on the costs and benefits of lay-date variation in tree swallows.

Animals must balance various costs and benefits when deciding when to breed. The costs and benefits of breeding at different times have received much attention, but most studies have been limited to investigating short-term season-to-season fitness effects. However, breeding early, versus late, in a season may influence lifetime fitness over many years, trading off in complex ways across the breeder's lifespan. In this study, we examined the complete life histories of 867 female tree swallows (Tachycineta bicolor) breeding in Ithaca, New York, between 2002 and 2016. Earlier breeders outperformed later breeders in short-term measures of reproductive output and offspring quality. Though there were weak indications that females paid long-term future survival costs for breeding early, lifetime fledgling output was markedly higher overall in early-breeding birds. Importantly, older females breeding later in the season did not experience compensating life history advantages that suggested an alternative equal-fitness breeding strategy. Rather, most or all of the swallows appear to be breeding as early as they can, and differences in lay dates appear to be determined primarily by differences in individual quality or condition. Lay date had a significant repeatability across breeding attempts by the same female, and the first lay date of females fledged in our population was strongly influenced by the first lay date of their mothers, indicating the potential for ongoing selection on lay date. By examining performance over the entire lifespan of a large number of individuals, we were able to clarify the relationship between timing of breeding and fitness and gain new insight into the sources of variability in this important life history trait.

Differences in perceived predation risk associated with variation in relative size of extra-pair and within-pair offspring.

Extra-pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra-pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra-pair and within-pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer-winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer-winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra-pair and within-pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.

The environmental and genetic determinants of chick telomere length in Tree Swallows (Tachycineta bicolor).

Conditions during early life can have dramatic effects on adult characteristics and fitness. However, we still know little about the mechanisms that mediate these relationships. Telomere shortening is one possibility. Telomeres are long sequences of DNA that protect the ends of chromosomes. They shorten naturally throughout an individual's life, and individuals with short telomeres tend to have poorer health and reduced survival. Given this connection between telomere length (TL) and fitness, natural selection should favor individuals that are able to retain longer telomeres for a greater portion of their lives. However, the ability of natural selection to act on TL depends on the extent to which genetic and environmental factors influence TL. In this study, we experimentally enlarged broods of Tree Swallows (Tachycineta bicolor) to test the effects of demanding early-life conditions on TL, while simultaneously cross-fostering chicks to estimate heritable genetic influences on TL. In addition, we estimated the effects of parental age and chick sex on chick TL. We found that TL is highly heritable in Tree Swallow chicks, and that the maternal genetic basis for TL is stronger than is the paternal genetic basis. In contrast, the experimental manipulation of brood size had only a weak effect on chick TL, suggesting that the role of environmental factors in influencing TL early in life is limited. There was no effect of chick sex or parental age on chick TL. While these results are consistent with those reported in some studies, they are in conflict with others. These disparate conclusions might be attributable to the inherent complexity of telomere dynamics playing out differently in different populations or to study-specific variation in the age at which subjects were measured.

The role of weather in mediating the effect of mercury exposure on reproductive success in tree swallows.

Mercury is a heavy metal that has contaminated countless ecosystems throughout the world. A large body of literature has documented reproductive, physiological, and behavioral impairments associated with mercury exposure in laboratory settings, but whether and how such effects are manifest in free-living populations remains poorly understood. The purpose of this study was to evaluate whether tree swallow (Tachycineta bicolor) breeding success at a site with high mercury exposure varied with ambient temperature or precipitation at various points in the breeding cycle. Tree swallows nesting along the South River had significantly elevated blood total mercury (mean ± SE: 3.03 ± 0.15 µg/g) compared to swallows breeding on reference sites (mean ± SE: 0.16 ± 0.005 µg/g). These high levels of mercury were associated with reduced hatching and fledging success, and contaminated birds produced approximately one less fledgling per nest than their reference counterparts. The magnitude of this difference was weather-dependent: unusually high ambient temperatures encountered early in the nestling period were associated with reduced reproductive output in contaminated, but not in reference, birds. In contrast, little effect of mercury on success of nestlings was observed when temperatures were cooler, and precipitation also had no detectable interaction with mercury. These results provide insight into mechanisms underlying reproductive effects of mercury. In addition, these findings underscore the importance of considering variable environmental conditions when assessing effects of contaminants on free-living wildlife. In particular, projections about the effects of global climate change on ecotoxicological impacts must take into account the kinds of weather-mediated effect demonstrated here.

Stability of mercury concentrations in frozen avian blood samples.

It is unclear whether mercury concentration in wildlife tissues changes appreciably after lengthy frozen storage. To test whether such freezer-archived samples are stable, small (~10-50 µL) avian blood samples stored in capped glass capillary tubes were analyzed for total mercury concentration, and then reanalyzed after being frozen for up to 3 years. Mercury concentrations increased 6% on average over the 3 year period, but time spent frozen explained only 11% of the variation between measurements. This small amount of change suggests that archived blood samples remain useful for at least several years.

Mercury exposure and survival in free-living tree swallows (Tachycineta bicolor).

Mercury has become a ubiquitous contaminant in food chains worldwide. A large body of literature detailing bioaccumulation and effects on birds has revealed the potential for mercury to adversely impact avian physiology and reproduction. However, the extent to which these effects impair survival remains poorly understood. The objective of this study was to determine whether mercury exposure was associated with reduced annual survivorship in tree swallows (Tachycineta bicolor) breeding at a site with legacy industrial contamination. From 2005 to 2008, we captured and marked 932 adult swallows. We used Cormack-Jolly-Seber models and an information-theoretic approach to test our hypotheses that adult survival varied by sex, breeding location, and cumulative individual mercury exposure. Blood mercury was significantly elevated on contaminated sites (2005-2007 combined mean ± SE: 2.84 ± 0.09 µg/g; reference: 0.17 ± 0.01 µg/g). Model-averaged estimates of female apparent survival ranged from 0.483 to 0.488 on reference sites and 0.473 to 0.477 on contaminated sites. For males, apparent survival ranged from 0.451 to 0.457 on reference sites and 0.444 to 0.448 on contaminated sites. Thus, we observed approximately a 1% difference in survival between mercury-contaminated and reference sites. Such a small difference is unlikely to impact population viability in this short-lived species; however, some songbirds accumulate mercury to a greater degree than tree swallows and do not possess the migratory behavior that removes swallows to less contaminated areas for the majority of the year. Identifying whether such species are at risk of suffering biologically significant reductions in survival should become a focus of future research.

Compromised immune competence in free-living tree swallows exposed to mercury.

Mercury is a pervasive environmental contaminant and a well-documented immunosuppressor. However, little is known about the effects of mercury contamination on health of free-living vertebrate populations. The South River in Virginia, USA was heavily contaminated with industrial mercury from 1929 to 1950, and recent studies have documented high levels of circulating mercury in riparian songbirds breeding below the site of contamination. Here we used two standardized immune assays, mitogen-induced swelling in response to phytohaemagglutinin (PHA) and antibody response to sheep red blood cells (SRBCs), to test for effects of mercury toxicity on the immune system of female tree swallows (Tachycineta bicolor) which feed on terrestrial and aquatic insects along the contaminated waterway. We found that females breeding at mercury-contaminated sites mounted significantly weaker PHA-induced swelling responses than those at reference sites in both years of study. However, among females on the contaminated sites, individual bloodstream mercury concentration did not predict the extent of mitogen-induced swelling. We did not detect any differences between reference and contaminated females in the strength of antibody responses to SRBCs, but sample sizes for this assay were significantly smaller. Overall, our results suggest that mercury toxicity can exert sub-lethal immunosuppression in free-living, insectivorous songbirds. The potential fitness consequences of the detected differences in immunocompetence caused by mercury toxicity warrant further study.

The movement of aquatic mercury through terrestrial food webs.

Mercury has contaminated rivers worldwide, with health consequences for aquatic organisms and humans who consume them. Researchers have focused on aquatic birds as sentinels for mercury. However, trophic transfer between adjacent ecosystems could lead to the export of aquatic mercury to terrestrial habitats. Along a mercury-contaminated river in Virginia, United States, terrestrial birds had significantly elevated levels of mercury in their blood, similar to their aquatic-feeding counterparts. Diet analysis revealed that spiders delivered much of the dietary mercury. We conclude that aquatic mercury pollution can move into terrestrial habitats, where it biomagnifies to levels in songbirds that may cause adverse effects. Rivers contaminated with mercury may pose a threat to the many bird species that feed on predatory invertebrates in adjacent riparian habitats.